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In the world of Mouse Guard, mice struggle to live safely and prosper amongst harsh conditions and a host of predators. Thus the Mouse Guard was formed: more than just soldiers that fight off intruders, they are guides for common mice looking to journey without confrontation from one hidden village to another. The Guard patrol borders, find safeways and paths through dangerous territories and treacherous terrain, watch weather patterns, and keep the Mouse Territories free of predatory infestation. They do so with fearless dedication so that they might not just exist, but truly live.

A mouse peddling grain took the path from Rootwallow to Barkstone alone, but never arrived at his destination. Mouse Guard members Saxon, Kenzie and Lieam are dispatched by Gwendolyn, head of the Mouse Guard to find him. It is quickly uncovered that the missing merchant mouse was devoured by a snake, which the three Guard members dispatch, but the plot thickens as the merchant is revealed as a traitor; carrying a detailed map of Lockhaven, home of the Mouse Guard.

While Guard members Saxon, Kenzie and Lieam were tracking the path of the grain merchant, Gwendolyn has sent word to another of the Guard, Sadie. Sadie, who once watched the shoreline region of the Mouse Territories, is to make contact with another missing mouse, Guard member Conrad, as there have been no outgoing communications from his northern shoreline dwelling Calogero.

Sadie arrives at Calogero to find it abandoned, or so it appears. She is quickly met by the peg-legged Conrad, who relates that the grain merchant is a traitor who would meet his mysterious master, who always remained in the shadows at Calogero. The duo plan to leave for Lockhaven at first light to warn them, but are surrounded the following morning by crabs. Conrad sacrifices himself to the crabs so that Sadie may have a chance to escape and warn the Mouse Guard of the traitor.

Saxon, Kenzie and Lieam, having abandoned the grain cart, have opted to take a lesser known path to the city of Barkstone in hopes to keep as low a profile as possible. What worries them more than knowing of a traitor, is not knowing who the traitor is. They are unaware of the information Sadie carries with her to Lockhaven, nor the fate of fellow Guard Conrad.

Arriving at the mouse city of Barkstone, Saxon, Kenzie and Lieam are forced to create a diversion to avoid watchful eyes. Kenzie and Saxon perform a duel between themselves while Lieam attempts to blend in with the townsmice. Lieam's investigation takes an unexpected twist when he uncovers the Axe, a well-organized anti-Guard group.

Hiding within the ranks of the mysterious militia known only as the Axe, Lieam is unaware that his Guard companions, Kenzie and Saxon, have been left for dead outside Barkstone's gates. Celanawe, a hermit and stranger of the mouse cities, retrieves and drags them to his secluded home.

The hermit Celanawe proclaims himself to be none other than the Black Axe, famed champion of the Mouse Guard who has been long presumed dead. Saxon, escaping his bonds, engages in combat with Celanawe, which results in the hermit's house burning down, but not before Kenzie is able to convince Celanawe that they must work together to stop the Axe. The Black Axe's legendary axe has been pilfered, which the two Guard mice agree to help recover. Elsewhere, Lieam is uncovered by the Axe as a spy and he realizes that the Axe's leader has a familiar voice.

The Axe marches on Lockhaven with the captive Lieam. While tracking the treacherous Axe army, Saxon and Kenzie find a new ally in an old hermit mouse named Celenawe, claiming to be the ancient hero of mice: the Black Axe. His fate intertwined with two of the Guard's finest, he offers to aide them in their pursuit, hoping to hold them to their word of retrieving his missing axe.

Midnight, the Mouse Guard's weaponsmith, is revealed to be the commander of the Axe army. He claims that "The Guard is useless...Gwendolyn exploits us. Cities, towns, and villages hold all the power. And Guard mice are their pawns. The territories need one sole leader. One who can offer security and prosperity. One who is not afraid to hunt down our predators. One who is more than a mere Guard mouse." Midnight then relates a tale of his discovery of the fabled Black Axe, which he accidentally uncovered the previous year in a secret room below the armory that housed a record of The Black Axe.

As Saxon and Kenzie travel with Celenawe, they privately discuss whether they think the old hermit is indeed the Black Axe. Celenawe continues to impress the Guard mice, not only setting the pace for their tracking but detouring them to higher ground and near a stockpile of weapons Kenzie made years before.

Sadie makes her way to Lockhaven successfully, beating both the Axe army and the Guard's mice tracking them to the gates. She warns the mice inside of the impending treachery and Lockhaven immediately locks itself down.

Midnight's army reaches Lockhaven as the Guardsmice inside try to stave off the invasion. Kenzie and Celanawe convince Saxon not to try attacking the army head on.

As the Axe assault Lockhaven, Midnight and several of his followers are able to get inside before the portcullis is dropped. Midnight nearly succeeds in killing Gwendolyn but is thwarted by the timely arrival of Celenawe while the Axe army is held off and defeated. Midnight is banished beyond the scent boundaries of the Mouse Territories to certain death while Lockhaven settles down for the winter and Celenawe returns to the Guard.

Both the hardcover and the paperback include several pages of previously unreleased material. The paperback includes an additional eight pages of "pin-up" art by Petersen himself (not to be confused with the guest pin ups which are also included in both editions).